Domain structure and denaturation of a dimeric mip-like peptidyl-prolyl cis-trans isomerase from Escherichia coli

Biochemistry

Volumn 51, Issue 6, 2012, Pages 1223-1237

  Jana, Biswanath ^a   Bandhu, Amitava ^a   Mondal, Rajkrishna ^a   Biswas, Anindya ^a   Sau, Keya ^b   Sau, Subrata ^a  

^a BOSE INSTITUTE   (India)

^b HALDIA INSTITUTE OF TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; CIS-TRANS; DOMAIN STRUCTURE; GUANIDINE HYDROCHLORIDE; IMMUNOSUPPRESSIVE DRUGS; ISOMERASES; LEGIONELLA; LIMITED PROTEOLYSIS; MODEL PROTEINS; MOLECULAR DIMENSIONS; MOLTEN GLOBULE; MULTIMERIC; N-TERMINAL DOMAINS; RECOMBINANT E. COLI; REFOLDING; TRANSITION STATE; TWO DOMAINS; TWO-STATE; TWO-STEP MECHANISMS; VIRULENCE FACTORS;

ESCHERICHIA COLI; METABOLISM; UREA;

RECOMBINANT PROTEINS;

ESCHERICHIA COLI PROTEIN; GUANIDINE; PEPTIDYLPROLYL ISOMERASE; PROTEIN HIS FKBP22; UNCLASSIFIED DRUG; UREA;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; EQUILIBRIUM CONSTANT; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN UNFOLDING;

BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; PROTEIN DENATURATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; SEQUENCE HOMOLOGY, AMINO ACID; TACROLIMUS; TACROLIMUS BINDING PROTEINS; VIRULENCE FACTORS;

ESCHERICHIA COLI; LEGIONELLA;

EID: 84856883486     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2015037     Document Type: Article

References (52)

1. Gothel, S. F. and Marahiel, M. A. (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts Cell. Mol. Life Sci. 55, 423-436 (Pubitemid 29178881)
2. Rahfeld, J. U., Rucknagel, K. P., Stoller, G., Horne, S. M., Schierhorn, A., Young, K. D., and Fischer, G. (1996) Isolation and amino acid sequence of a new 22-kDa FKBP-like peptidyl-prolyl cis/trans -isomerase of Escherichia coli. Similarity to Mip-like proteins of pathogenic bacteria J. Biol. Chem. 271, 22130-22138 (Pubitemid 26303844)
3. Engleberg, N. C., Carter, C., Weber, D. R., Cianciotto, N. P., and Eisenstein, B. I. (1989) DNA sequence of mip, a Legionella pneumophila gene associated with macrophage infectivity Infect. Immun. 57, 1263-1270 (Pubitemid 19087876)
4. Lundemose, A. G., Kay, J. E., and Pearce, J. H. (1993) Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection Mol. Microbiol. 7, 777-783 (Pubitemid 23090359)
5. Moro, A., Ruiz-Cabello, F., Fernandez-Cano, A., Stock, R. P., and Gonzalez, A. (1995) Secretion by Trypanosoma cruzi of a peptidyl-prolyl cis-trans isomerase involved in cell infection EMBO J. 14, 2483-2490
6. Horne, S. M. and Young, K. D. (1995) Escherichia coli and other species of the Enterobacteriaceae encode a protein similar to the family of Mip-like FK506-binding proteins Arch. Microbiol. 163, 357-365
7. Ramm, K. and Pluckthun, A. (2000) The periplasmic Escherichia coli peptidylprolyl cis,trans -isomerase FkpA. II. Isomerase-independent chaperone activity in vitro J. Biol. Chem. 275, 17106-17113 (Pubitemid 30398955)
8. Horne, S. M., Kottom, T. J., Nolan, L. K., and Young, K. D. (1997) Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen Infect. Immun. 65, 806-810 (Pubitemid 27053256)
9. Suzuki, Y., Haruki, M., Takano, K., Morikawa, M., and Kanaya, S. (2004) Possible involvement of an FKBP family member protein from a psychrotrophic bacterium Shewanella sp. SIB1 in cold-adaptation Eur. J. Biochem. 271, 1372-1381 (Pubitemid 38519614)
10. Leuzzi, R., Serino, L., Scarselli, M., Savino, S., Fontana, M. R., Monaci, E., Taddei, A., Fischer, G., Rappuoli, R., and Pizza, M. (2005) Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages Mol. Microbiol. 58, 669-681 (Pubitemid 41532466)
11. Zang, N., Tang, D. J., Wei, M. L., He, Y. Q., Chen, B., Feng, J. X., Xu, J., Gan, Y. Q., Jiang, B. L., and Tang, J. L. (2007) Requirement of a mip -like gene for virulence in the phytopathogenic bacterium Xanthomonas campestris pv. campestris Mol. Plant-Microbe Interact. 20, 21-30 (Pubitemid 44956908)
12. Riboldi-Tunnicliffe, A., Konig, B., Jessen, S., Weiss, M. S., Rahfeld, J., Hacker, J., Fischer, G., and Hilgenfeld, R. (2001) Crystal structure of Mip, a prolylisomerase from Legionella pneumophila Nat. Struct. Biol. 8, 779-783 (Pubitemid 32803596)
13. Saul, F. A., Arie, J. P., Vulliez-le Normand, B., Kahn, R., Betton, J. M., and Bentley, G. A. (2004) Structural and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity J. Mol. Biol. 335, 595-608 (Pubitemid 37532659)
14. Köhler, R., Fanghanel, J., Konig, B., Luneberg, E., Frosch, M., Rahfeld, J. U., Hilgenfeld, R., Fischer, G., Hacker, J., and Steinert, M. (2003) Biochemical and functional analyses of the Mip protein: Influence of the N-terminal half and of peptidylprolyl isomerase activity on the virulence of Legionella pneumophila Infect. Immun. 71, 4389-4397 (Pubitemid 36919904)
15. Ceymann, A., Horstmann, M., Ehses, P., Schweimer, K., Paschke, A., Michael Steinert, M., and Faber, C. (2008) Solution structure of the Legionella pneumophila Mip-rapamycin complex BMC Struct. Biol. 8, 17
16. Suzuki, Y., Takano, K., and Kanaya, S. (2005) Stabilities and activities of the N- and C-domains of FKBP22 from a psychrotrophic bacterium overproduced in Escherichia coli FEBS J. 272, 632-642 (Pubitemid 40208868)
17. Budiman, C., Bando, K., Angkawidjaja, C., Koga, Y., Takano, K., and Kanaya, S. (2009) Engineering of monomeric FK506-binding protein 22 with peptidyl prolyl cis-trans isomerase. Importance of a V-shaped dimeric structure for binding to protein substrate FEBS J. 276, 4091-4101
18. Jaenicke, R. (2000) Stability and stabilization of globular proteins in solution J. Biotechnol. 79, 193-203 (Pubitemid 30365192)
19. Kim, P. S. and Baldwin, R. L. (1990) Intermediates in the folding reactions of small proteins Annu. Rev. Biochem. 59, 631-660
20. Neet, K. E. and Timm, D. E. (1994) Conformational stability of dimeric proteins: Quantitative studies by equilibrium denaturation Protein Sci. 3, 2167-2174
21. Egan, D. A., Logan, T. M., Liang, H., Matayoshi, E., Fesik, S. W., and Holzman, T. F. (1993) Equilibrium denaturation of recombinant human FK binding protein in urea Biochemistry 32, 1920-1927 (Pubitemid 23086040)
22. Main, E. R., Fulton, K. F., and Jackson, S. E. (1999) Folding pathway of FKBP12 and characterisation of the transition state J. Mol. Biol. 291, 429-444 (Pubitemid 29381437)
23. Liu, C. P., Li, Z. Y., Huang, G. C., Perrett, S., and Zhou, J. M. (2005) Two distinct intermediates of trigger factor are populated during guanidine denaturation Biochimie 87, 1023-1031 (Pubitemid 41377162)
24. Zarnt, T., Tradler, T., Stoller, G., Scholz, C., Schmid, F. X., and Fischer, G. (1997) Modular structure of the trigger factor required for high activity in protein folding J. Mol. Biol. 271, 827-837 (Pubitemid 27376057)
25. Mitra, D., Mukherjee, S., and Das, A. K. (2006) Cyclosporin A binding to Mycobacterium tuberculosis peptidyl-prolyl cis-trans isomerase A: Investigation by CD, FTIR and fluorescence spectroscopy FEBS Lett. 580, 6846-6860 (Pubitemid 44909125)
26. Arai, M. and Kuwajima, K. (2000) Role of the molten globule state in protein folding Adv. Protein Chem. 53, 209-282 (Pubitemid 34194295)
27. Sambrook, J. and Russell, D. W. (2001) Molecular cloning: A laboratory manual, 3rd ed., Cold Spring Harbor Laboratory Press, Plainview, NY.
28. Ausubel, F. M. (1987) Current protocols in molecular biology, Greene Publishing Associates and Wiley-Interscience, New York.
29. Bandhu, A., Ganguly, T., Jana, B., Mondal, R., and Sau, S. (2010) Regions and residues of an asymmetric operator DNA interacting with the monomeric repressor of temperate mycobacteriophage L1 Biochemistry 49, 4235-4243
30. Ganguly, T., Das, M., Bandhu, A., Chanda, P. K., Jana, B., Mondal, R., and Sau, S. (2009) Physicochemical properties and distinct DNA binding capacity of the repressor of temperate Staphylococcus aureus phage φ11 FEBS J. 276, 1975-1985
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
32. Wear, M. A., Patterson, A., and Walkinshaw, M. D. (2007) A kinetically trapped intermediate of FK506 binding protein forms in vitro: Chaperone machinery dominates protein folding in vivo Protein Expression Purif. 51, 80-95 (Pubitemid 44822661)
33. Lakowicz, J. R. (1999) Principles of fluorescence spectroscopy, 2nd ed., Kluwer Academic/Plenum, New York.
34. Wessel, D. and Flugge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids Anal. Biochem. 138, 141-143 (Pubitemid 14146660)
35. Creighton, T. E. (1997) Protein Structure: A Practical Approach, 2nd ed., IRL Press at Oxford University Press, New York.
36. Eftink, M. R. and Ghiron, C. A. (1981) Fluorescence quenching studies with proteins Anal. Biochem. 114, 199-227
37. Goldenberg, D. P. and Creighton, T. E. (1984) Gel electrophoresis in studies of protein conformation and folding Anal. Biochem. 138, 1-18
38. Pace, C. N. and Shaw, K. L. (2000) Linear extrapolation method of analyzing solvent denaturation curves Proteins Suppl. 4, 1-7
39. Chakrabarty, S. P. and Balaram, H. (2010) Reversible binding of zinc in Plasmodium falciparum Sir2: Structure and activity of the apoenzyme Biochim. Biophys. Acta 1804, 1743-1750
40. Fontana, A., de Laureto, P. P., Spolaore, B., Frare, E., Picotti, P., and Zambonin, M. (2004) Probing protein structure by limited proteolysis Acta Biochim. Pol. 51, 299-321 (Pubitemid 38969296)
41. Royer, C. A., Mann, C. J., and Matthews, C. R. (1993) Resolution of the fluorescence equilibrium unfolding profile of trp aporepressor using single tryptophan mutants Protein Sci. 2, 1844-1852 (Pubitemid 23328539)
42. Gianazza, E., Miller, I., Eberini, I., and Castiglioni, S. (1999) Low-tech electrophoresis, small but beautiful, and effective: Electrophoretic titration curves of proteins Electrophoresis 20, 1325-1338 (Pubitemid 29299979)
43. Siddiqui, K. S., Feller, G., D'Amico, S., Gerday, C., Giaquinto, L., and Cavicchioli, R. (2005) The active site is the least stable structure in the unfolding pathway of a multidomain cold-adpated amylase J. Bacteriol. 187, 6197-6205 (Pubitemid 41262816)
44. Park, C. Y. and Bedouelle, H. (1998) Dimeric tyrosyl-tRNA synthetase from Bacillus stearothermophilus unfolds through a monomeric intermediate J. Biol. Chem. 273, 18052-18059
45. Agarwalla, A., Gokhale, R. S., Santi, D. V., and Balaram, P. (1996) Covalent tethering of the dimer interface annuls aggregation in thymidylate synthase Protein Sci. 5, 270-277 (Pubitemid 26054283)
46. Cellini, B., Bertoldi, M., Montioli, R., Laurents, D. V., Paiardini, A., and Voltattorni, C. B. (2006) Dimerization and folding processes of Treponema denticola cystalysin: The role of pyridoxal 5′-phosphate Biochemistry 45, 14140-14154 (Pubitemid 44846203)
47. Kim, D. H., Nam, G. H., Jang, D. S., Yun, S., Choi, G., Lee, H. C., and Choi, K. Y. (2001) Roles of dimerization in folding and stability of ketosteroid isomerase from Pseudomonas putida biotype B Protein Sci. 10, 741-752 (Pubitemid 32240500)
48. Najera, H., Costas, M., and Fernandez-Velasco, D. A. (2003) Thermodynamic characterization of yeast triosephosphate isomerase refolding: Insights into the interplay between function and stability as reasons for the oligomeric nature of the enzyme Biochem. J. 370, 785-792 (Pubitemid 36399070)
49. Akhtar, M. S., Ahmad, A., and Bhakuni, V. (2002) Guanidinium chloride- and urea-induced unfolding of the dimeric enzyme glucose oxidase Biochemistry 41, 3819-3827 (Pubitemid 34224697)
50. Rashid, F., Sharma, S., and Bano, B. (2005) Comparison of guanidine hydrochloride (GdnHCl) and urea denaturation on inactivation and unfolding of human placental cystatin (HPC) Protein J. 24, 283-292 (Pubitemid 41609501)
51. Singh, A. R., Joshi, S., Arya, R., Kayastha, A. M., and Saxena, J. K. (2010) Guanidine hydrochloride and urea-induced unfolding of Brugia malayi hexokinase Eur. Biophys. J. 39, 289-297
52. Nandi, P. K. and Robinson, D. R. (1984) Effects of urea and guanidine hydrochloride on peptide and non-polar groups Biochemistry 23, 6661-6668